Macrophage Activation and Polarization: Nomenclature and Experimental Guidelines

Immunity

Volumn 41, Issue 1, 2014, Pages 14-20

  Murray, Peter ^a   Allen, Judith ^b   Biswas, Subhra ^c   Fisher, Edward ^d   Gilroy, Derek ^e   Goerdt, Sergij ^f   Gordon, Siamon ^g   Hamilton, John ^h   Ivashkiv, Lionel ⁱ   Lawrence, Toby ^j   Locati, Massimo ^k   Mantovani, Alberto ^k   Martinez, Fernando ^l   Mege, Jean Louis ^m   Mosser, David ⁿ   Natoli, Gioacchino ^o   Saeij, Jeroen ^p   Schultze, Joachim ^q   Shirey, KariAnn ^r   Sica, Antonio ^s,t   Suttles, Jill ^u   Udalova, Irina ^v   vanGinderachter, Jo ^w,x   Vogel, Stefanie ^r   Wynn, Thomas ^y   more..

^a ST JUDE CHILDREN S RESEARCH HOSPITAL   (United States)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

^c AGENCY FOR SCIENCE   (Singapore)

^d NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^e UNIVERSITY COLLEGE LONDON   (United Kingdom)

^f UNIVERSITY OF HEIDELBERG   (Germany)

^g UNIVERSITY OF OXFORD   (United Kingdom)

^h UNIVERSITY OF MELBOURNE   (Australia)

ⁱ Department of Molecular Biology and Genetics   (United States)

^j CENTRE D IMMUNOLOGIE DE MARSEILLE LUMINY   (France)

^k UNIVERSITY OF MILAN   (Italy)

^l UNIVERSITY OF OXFORD   (United Kingdom)

^m AIX MARSEILLE UNIVERSITY   (France)

ⁿ UNIVERSITY OF MARYLAND   (United States)

^o EUROPEAN INSTITUTE OF ONCOLOGY   (Italy)

^p MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^q UNIVERSITY OF BONN   (Germany)

^r UNIVERSITY OF MARYLAND SCHOOL OF MEDICINE   (United States)

^s HUMANITAS CLINICAL AND RESEARCH CENTER   (Italy)

^t UNIVERSITY OF EASTERN PIEDMONT   (Italy)

^u University of Louisville School of Medicine   (United States)

^v UNIVERSITY OF OXFORD   (United Kingdom)

^w VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^x DEPARTMENT OF PLANT SYSTEMS BIOLOGY   (Belgium)

^y NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; GUIDELINES AS TOPIC; HUMANS; MACROPHAGE ACTIVATION; MACROPHAGE COLONY-STIMULATING FACTOR; MACROPHAGES; MICE; RESEARCH; TERMINOLOGY AS TOPIC;

EID: 84904394690     PISSN: 10747613     EISSN: 10974180     Source Type: Journal    
DOI: 10.1016/j.immuni.2014.06.008     Document Type: Review

References (49)

1. Ai D., Jiang H., Westerterp M., Murphy A.J., Wang M., Ganda A., Abramowicz S., Welch C., Almazan F., Zhu Y., et al. Disruption of mammalian target of rapamycin complex 1 in macrophages decreases chemokine gene expression and atherosclerosis. Circ. Res. 2014, 114:1576-1584.
2. Arranz A., Doxaki C., Vergadi E., Martinez de la Torre Y., Vaporidi K., Lagoudaki E.D., Ieronymaki E., Androulidaki A., Venihaki M., Margioris A.N., et al. Akt1 and Akt2 protein kinases differentially contribute to macrophage polarization. Proc. Natl. Acad. Sci. USA 2012, 109:9517-9522.
3. Biswas S.K., Mantovani A. Macrophage plasticity and interaction with lymphocyte subsets: cancer as a paradigm. Nat. Immunol. 2010, 11:889-896.
4. Byles V., Covarrubias A.J., Ben-Sahra I., Lamming D.W., Sabatini D.M., Manning B.D., Horng T. The TSC-mTOR pathway regulates macrophage polarization. Nat. Commun. 2013, 4:2834.
5. Chawla A. Control of macrophage activation and function by PPARs. Circ. Res. 2010, 106:1559-1569.
6. Date D., Das R., Narla G., Simon D.I., Jain M.K., Mahabeleshwar G.H. Kruppel-like transcription factor 6 regulates inflammatory macrophage polarization. J.Biol. Chem. 2014, 289:10318-10329.
7. Edwards J.P., Zhang X., Frauwirth K.A., Mosser D.M. Biochemical and functional characterization of three activated macrophage populations. J.Leukoc. Biol. 2006, 80:1298-1307.
8. El Kasmi K.C., Qualls J.E., Pesce J.T., Smith A.M., Thompson R.W., Henao-Tamayo M., Basaraba R.J., König T., Schleicher U., Koo M.S., et al. Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat. Immunol. 2008, 9:1399-1406.
9. Fairbairn L., Kapetanovic R., Sester D.P., Hume D.A. The mononuclear phagocyte system of the pig as a model for understanding human innate immunity and disease. J.Leukoc. Biol. 2011, 89:855-871.
10. Festuccia W.T., Pouliot P., Bakan I., Sabatini D.M., Laplante M. Myeloid-specific Rictor deletion induces M1 macrophage polarization and potentiates invivo pro-inflammatory response to lipopolysaccharide. PLoS ONE 2014, 9:e95432.
11. Fleetwood A.J., Dinh H., Cook A.D., Hertzog P.J., Hamilton J.A. GM-CSF- and M-CSF-dependent macrophage phenotypes display differential dependence on type I interferon signaling. J.Leukoc. Biol. 2009, 86:411-421.
12. Gautier E.L., Shay T., Miller J., Greter M., Jakubzick C., Ivanov S., Helft J., Chow A., Elpek K.G., Gordonov S., et al. Gene-expression profiles and transcriptional regulatory pathways that underlie the identity and diversity of mouse tissue macrophages. Nat. Immunol. 2012, 13:1118-1128. Immunological Genome Consortium.
13. Gordon S., Martinez F.O. Alternative activation of macrophages: mechanism and functions. Immunity 2010, 32:593-604.
14. Gratchev A., Kzhyshkowska J., Kannookadan S., Ochsenreiter M., Popova A., Yu X., Mamidi S., Stonehouse-Usselmann E., Muller-Molinet I., Gooi L., Goerdt S. Activation of a TGF-beta-specific multistep gene expression program in mature macrophages requires glucocorticoid-mediated surface expression of TGF-beta receptor II. J.Immunol. 2008, 180:6553-6565.
15. Gundra U.M., Girgis N.M., Ruckerl D., Jenkins S., Ward L.N., Kurtz Z.D., Wiens K.E., Tang M.S., Basu-Roy U., Mansukhani A., et al. Alternatively activated macrophages derived from monocytes and tissue macrophages are phenotypically and functionally distinct. Blood 2014, 123:e110-e122.
16. Ivashkiv L.B. Epigenetic regulation of macrophage polarization and function. Trends Immunol. 2013, 34:216-223.
17. Joshi S., Singh A.R., Zulcic M., Bao L., Messer K., Ideker T., Dutkowski J., Durden D.L. Rac2 controls tumor growth, metastasis and M1-M2 macrophage differentiation invivo. PLoS ONE 2014, 9:e95893.
18. Krausgruber T., Blazek K., Smallie T., Alzabin S., Lockstone H., Sahgal N., Hussell T., Feldmann M., Udalova I.A. IRF5 promotes inflammatory macrophage polarization and TH1-TH17 responses. Nat. Immunol. 2011, 12:231-238.
19. Lang R., Patel D., Morris J.J., Rutschman R.L., Murray P.J. Shaping gene expression in activated and resting primary macrophages by IL-10. J.Immunol. 2002, 169:2253-2263.
20. Lawrence T., Natoli G. Transcriptional regulation of macrophage polarization: enabling diversity with identity. Nat. Rev. Immunol. 2011, 11:750-761.
21. Mantovani A., Sica A., Locati M. Macrophage polarization comes of age. Immunity 2005, 23:344-346.
22. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
23. Martinez F.O., Gordon S. The M1 and M2 paradigm of macrophage activation: time for reassessment. F1000Prime Rep 2014, 6:13.
24. Martinez F.O., Sica A., Mantovani A., Locati M. Macrophage activation and polarization. Front. Biosci. 2008, 13:453-461.
25. Martinez F.O., Helming L., Milde R., Varin A., Melgert B.N., Draijer C., Thomas B., Fabbri M., Crawshaw A., Ho L.P., et al. Genetic programs expressed in resting and IL-4 alternatively activated mouse and human macrophages: similarities and differences. Blood 2013, 121:e57-e69.
26. Mills C.D. M1 and M2 Macrophages: Oracles of Health and Disease. Crit. Rev. Immunol. 2012, 32:463-488.
27. Mills C.D., Kincaid K., Alt J.M., Heilman M.J., Hill A.M. M-1/M-2 macrophages and the Th1/Th2 paradigm. J.Immunol. 2000, 164:6166-6173.
28. Moore K.J., Sheedy F.J., Fisher E.A. Macrophages in atherosclerosis: a dynamic balance. Nat. Rev. Immunol. 2013, 13:709-721.
29. Mosser D.M., Edwards J.P. Exploring the full spectrum of macrophage activation. Nat. Rev. Immunol. 2008, 8:958-969.
30. Murray P.J., Wynn T.A. Obstacles and opportunities for understanding macrophage polarization. J.Leukoc. Biol. 2011, 89:557-563.
31. Murray P.J., Wynn T.A. Protective and pathogenic functions of macrophage subsets. Nat. Rev. Immunol. 2011, 11:723-737.
32. Nathan C., Ding A. Nonresolving inflammation. Cell 2010, 140:871-882.
33. Porta C., Rimoldi M., Raes G., Brys L., Ghezzi P., Di Liberto D., Dieli F., Ghisletti S., Natoli G., De Baetselier P., et al. Tolerance and M2 (alternative) macrophage polarization are related processes orchestrated by p50 nuclear factor kappaB. Proc. Natl. Acad. Sci. USA 2009, 106:14978-14983.
34. Rutschman R., Lang R., Hesse M., Ihle J.N., Wynn T.A., Murray P.J. Cutting edge: Stat6-dependent substrate depletion regulates nitric oxide production. J.Immunol. 2001, 166:2173-2177.
35. Sans-Fons M.G., Yeramian A., Pereira-Lopes S., Santamaría-Babi L.F., Modolell M., Lloberas J., Celada A. Arginine transport is impaired in C57Bl/6 mouse macrophages as a result of a deletion in the promoter ofSlc7a2 (CAT2), and susceptibility to Leishmania infection is reduced. J.Infect. Dis. 2013, 207:1684-1693.
36. Schroder K., Irvine K.M., Taylor M.S., Bokil N.J., Le Cao K.A., Masterman K.A., Labzin L.I., Semple C.A., Kapetanovic R., Fairbairn L., et al. Conservation and divergence in Toll-like receptor 4-regulated gene expressionin primary human versus mouse macrophages. Proc. Natl. Acad. Sci. USA 2012, 109:E944-E953.
37. Shirey K.A., Cole L.E., Keegan A.D., Vogel S.N. Francisella tularensis live vaccine strain induces macrophage alternative activation as asurvival mechanism. J.Immunol. 2008, 181:4159-4167.
38. Shirey K.A., Pletneva L.M., Puche A.C., Keegan A.D., Prince G.A., Blanco J.C., Vogel S.N. Control of RSV-induced lung injury by alternatively activated macrophages is IL-4R alpha-, TLR4-, and IFN-beta-dependent. Mucosal Immunol. 2010, 3:291-300.
39. Shirey K.A., Lai W., Pletneva L.M., Karp C.L., Divanovic S., Blanco J.C., Vogel S.N. Role of the lipoxygenase pathway in RSV-induced alternatively activated macrophages leading to resolution of lung pathology. Mucosal Immunol. 2014, 7:549-557.
40. Sieweke M.H., Allen J.E. Beyond stem cells: self-renewal of differentiated macrophages. Science 2013, 342:1242974.
41. Stein M., Keshav S., Harris N., Gordon S. Interleukin 4 potently enhances murine macrophage mannose receptor activity: a marker of alternative immunologic macrophage activation. J.Exp. Med. 1992, 176:287-292.
42. Stout R.D., Suttles J. Functional plasticity of macrophages: reversible adaptation to changing microenvironments. J.Leukoc. Biol. 2004, 76:509-513.
43. Stout R.D., Jiang C., Matta B., Tietzel I., Watkins S.K., Suttles J. Macrophages sequentially change their functional phenotype in response to changes in microenvironmental influences. J.Immunol. 2005, 175:342-349.
44. Taub D.D., Cox G.W. Murine Th1 and Th2 cell clones differentially regulate macrophage nitric oxide production. J.Leukoc. Biol. 1995, 58:80-89.
45. Warren M.K., Vogel S.N. Bone marrow-derived macrophages: development and regulation of differentiation markers by colony-stimulating factor and interferons. J.Immunol. 1985, 134:982-989.
46. Weichhart T., Costantino G., Poglitsch M., Rosner M., Zeyda M., Stuhlmeier K.M., Kolbe T., Stulnig T.M., Hörl W.H., Hengstschläger M., et al. The TSC-mTOR signaling pathway regulates the innate inflammatory response. Immunity 2008, 29:565-577.
47. Wynn T.A., Chawla A., Pollard J.W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496:445-455.
48. Xue J., Schmidt S.V., Sander J., Draffehn A., Krebs W., Quester I., De Nardo D., Gohel T.D., Emde M., Schmidleithner L., et al. Transcriptome-based network analysis reveals a spectrum model of human macrophage activation. Immunity 2014, 40:274-288.
49. Yue S., Rao J., Zhu J., Busuttil R.W., Kupiec-Weglinski J.W., Lu L., Wang X., Zhai Y. Myeloid PTEN deficiency protects livers from ischemia reperfusion injury by facilitating M2 macrophage differentiation. J.Immunol. 2014, 192:5343-5353.